Natural killer cells license dendritic cell cross-presentation of B lymphoma cell--associated antigens

Clin Cancer Res. 2005 Dec 15;11(24 Pt 1):8763-72. doi: 10.1158/1078-0432.CCR-05-0975.

Abstract

Purpose: Presentation of exogenous antigen by MHC class I molecules, or cross-presentation, is a property of dendritic cells, which is considered crucial for the priming of cytotoxic T-cell response to tumor antigens. However, the precise mechanisms of this process are not fully understood.

Experimental design and results: We show here in a human in vitro system, using B lymphoma cells as a tumor model, that the cross-presentation of cell-associated antigens to T cells by dendritic cells requires "help" from natural killer cells. When autologous dendritic cells that had taken up apoptotic B lymphoma cells and induced to a fully mature state were used to stimulate nonadherent cells of peripheral blood mononuclear cells from healthy donors, they induced strong cytotoxicity against B lymphoma cells in a HLA-A0201-restricted manner. The cells failed to induce cytotoxicity, however, when purified T cells were used as effector cells. Depletion of CD56+ cells, but not CD14+ or CD19+ cells, abrogated the cytotoxicity of nonadherent cells, showing that the help was provided by natural killer cells. Further, when natural killer cells were present in the cultures, a strong and persistent production of interleukin-18, but not interleukin-12 and interleukin-15, was observed. Blocking interleukin-18 significantly reduced the cytotoxicity of nonadherent cells against B lymphoma cells.

Conclusions: These results suggest that capture of tumor cells and a full maturation status of dendritic cells are not sufficient to cross-prime CD8 T cells. Effective cross-priming requires further activation of dendritic cells by natural killer cells and an abundant production of interleukin-18, which, along with other yet undefined mechanisms, contribute to the generation of CTL response against B-cell lymphoma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Blocking / pharmacology
  • Antigens, Neoplasm / analysis
  • Antigens, Neoplasm / immunology*
  • CD56 Antigen / analysis
  • CD56 Antigen / immunology
  • Cell Line, Tumor
  • Coculture Techniques
  • Cross-Priming / immunology*
  • Cytotoxicity, Immunologic / drug effects
  • Cytotoxicity, Immunologic / immunology*
  • Dendritic Cells / immunology*
  • Humans
  • Interleukin-18 / antagonists & inhibitors
  • Interleukin-18 / metabolism
  • Killer Cells, Natural / immunology*
  • Lymphocyte Depletion
  • Lymphoma, B-Cell / immunology*
  • Phagocytosis
  • T-Lymphocytes, Cytotoxic / immunology

Substances

  • Antibodies, Blocking
  • Antigens, Neoplasm
  • CD56 Antigen
  • Interleukin-18